A Comparison of Amphibian Communities Through Time and Place to Place

8/9/2019 A Comparison of Amphibian Communities Through Time and Place to Place

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Journal of Trop ical Ecology (1993) 9:409-433. With 2 figures

A ciimparison of amphibian communities

through time and from place to place in Bornean

forests

ROBERT F. INGER

and

HAROLD K. VORIS

Field Museum of Natural History, Chicago, Illinois, USA

ABSTR ACT. We sampled riparian frogs along 18 streams at eight localities in Borneo. At four of

these sites we samp led during more than one year. Altogether 49 spe cies were includ ed in our

study an d total sam ple size was 13,249. We measured overlap in spe cies occurrence s and arrays

of abund ances within and among loca lities. Variation over the time span of our study was minor

within com mun ities. Overlaps between streams at a locality were generally higher than overlaps

of pairs of streams from different loca lities. Environmental variation, particularly in stream width

and gradient, had a clear effect on both intra-and inter-locality overlaps. Although rainfall varied

between loca lities and within loca lities over time, that variation did not seem to affect overlaps

among or within com mun ities. Environmental factors did not accoun t for all differences in overlaps

between comm unities. Instead, regional proce sses, perhaps the timing of barriers or spec iation

events, appear to have been respon sible for geograph ic restrictions of several specie s, leading to

variation in overlap values.

KEY WORDS: anurans, Borneo, commun ity structure, community variation, Malaysia, rain

forests.

INTRODUCTION

When one looks at community structure within a relatively small area, the

significance ecologists attach to local phenomena, such as biotic interactions

and species-specific responses to environmental features, is understandable.

These are the most apparent phenomena, even if they are not always easy to

tease apart and evaluate. However, as Ricklefs (1987) observed, features of local

community structure may be strongly affected by regional processes, such as

barriers to dispersal, the history of speciation, and other phylogenetic events.

For certain aspects of community structure viewed at a regional scale, Hanski

( 1982) proposed a model relating distribution of species across sites to their

abundances. This model assumes that species populations fluctuate in stochastic

fashion over time in response to biotic interactions and environmental fluctu-

ations. In effect, local processes lead to regional patterns. A study by Gascon

( 1991) on larvae of Amazonian frogs shows the inter-play of local and regional

processes. These tadpoles had species-specific responses to abiotic habitat char-

acteristics and Gascon’s data give hints of biotic interactions, e.g. scarcity of

409


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410

ROBERT F. INGER AND HAROLD K. VORIS

co-occurrence of larval species, a typical local process. Yet the restriction of

‘

two larval forms to stream microhabitats is clearly a product of phylogenetic *

history. These two, Atelopus p&her and Centrolenella oyampiensis, belong to genera

J al l of whose larvae develop in streams (Duellman & Lynch 1969, McDiarmid,

1978) regardless of the distributions of other sympatric tadpoles of other genera.

4

Most studies of community structure in tropical amphibians have concen-

trated on a single, relatively restricted area (e.g. Crump 1971, Gascon 1991,

Heyer 1973, Inger 1969, Inger & Colwell 1977, Toft & Duellman 1979). That

concentration perhaps explains the primary focus on local processes. In this

paper we examine variation among Bornean amphibian communities across an

area approximately 700 km wide, which obliges us to consider regional processes

as well as local ones.

Our analysis is restricted to that segment of the Bornean amphibian commun-

ity occurring along rain forest streams, species that spend their entire li fe cycles

in this riparian habitat or that utilize streams for breeding and larval develop-

ment. We begin with examination of variation over a 22-year period at one site,

Nanga Tekalit, Sarawak (Figure 1, site 1 ), which provides a standard with

which to evaluate variation over space. We then consider factors associated

with variation from place to place.

1100

114O

1180

I

I I

I

1 I

Figure 1. Map show ing the eight local ities in the Malaysian states of Sarawak (numbers l-4) and Sabah

(numbers 5-8) on the island of Borneo. The localities are (1) Nanga Tekalit, (2) Segaham, (3) Pesu, (4)

Labang, (5) Mendolong, (6) Purulon , (7) Marak Parak, and (8) Danum.


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Variatibn among frog communities

411

SAMPLING SITES

Our sampling of stream frogs was conducted at eight localities in rain forests

below 800 m in Borneo in the Malaysian states of Sabah and Sarawak (Figure

1, Table 1). Distances between localities range from 35 to 640 km (Table 2).

Full details of these sites are given in Appendix A.

Sites differed in several ways:

(i) Topography. The only flat area was Labang (site 4, Figure 1). The rest

were hilly (e.g. Danum, site 8) to steep (Purulon and Segaham, sites 2 and

6).

(ii) Elevation. All except Purulon and Mendolong (site 5) were below 300 m

asl. The streams at Purulon are at 320-370 m and the one at Mendolong

at 750 m.

(iii) Vegetation. The entire area of Mendolong included in this study had been

selectively logged. The forest at Marak-Parak (site 7) was old (45-50 y)

secondary growth that now has a high closed canopy. Labang was covered

with flat, alluvia l forest. Most of the area at Pesu and all the area at the

remaining sites was well-drained, hil ly, and covered with primary diptero-

carp forest. There was a small area of swamp forest at Pesu (site 3), and

both Danum and Nanga Tekalit (site 1) had a few flat areas.

(iv) Rainfall. Amount of rainfall during sampling periods varied greatly from

site to site. The four in Sarawak had the most precipitation, with few

months having 300

mm.

(v) Streams. Regardless of amount of rainfall, al l streams in this study were

perennial. All became turbid after heavy rain, but only Sungai Seran at

Labang was continually turbid. Sungai Seran was also the only low gradi-

ent stream and the only one with a silt bottom. Stream widths vary from

3 to 25 m. Streams less than 8 m wide were under canopy, those 8-10 m

partially under canopy. Banks of even the largest streams were under trees.

MATERIALS AND METHODS

Field procedures

At each site work was divided between effort along streams and in the forest

proper. Data from the non-riparian work, which consisted of forest floor plots,

search of buttress-enclosed areas, and night transects through the forest, are

not used in this paper, but contribute to an understanding of the total fauna at

each site. The riparian work included collecting and observing tadpoles by day

and collecting and observing frogs during night transects. The data from the

night transects along fixed segments (250600 m) of streams form the basis of

this paper. On streams at four of the localities, we marked stations at 15-30 m

intervals with plastic flagging and recorded the position of each frog observed


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Table 1. The number of night stream transects and the number of anurans observed each year on each stream.

Locality Stream

First sample period Second sample period Third sample period

Year Transects Anurans Year Transects Anurans Year Transects Anurans

Labang Seran 1963 29 477

Nanga Tekalit Ensurai 1962 36 747 1970 5 295 1984 5 241

Sekentut 1962 36 772 1970 5 206 1984 5 247

Selubok 1962 15 640 1970 5 232

Set-bong 1962 36 1038 1970 5 377 1984 5 252

Lawan 1962 17 469

Wong 1962 12 319 1984 2 51

PeSU Pesu 1964 78 1775

Segaham Segaham 1984 13 612

Marok 1984 10 331

Danum Cabin 1989

4 97 1990 7 179 fz

P. Tambun 1986 5 476 1989 4 88

1990 7 306

S.Kalison 1989 7 194 1990 9 267

E;

W6S5 1986

4 213 1989 4 ’ 71 1990 4 122

206

F

Surinsin 1988 4

c

c

Marak Parak Mendolong 1987 5 234 1989 5 327 1990 5 291 ;

6 284

;:

Mendolong Kilampo n 1989

7 322 1990

Purulon Purulon 1989

6 257 1990 7 234


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Variation among frog communities

413

Table 2. Distances (km) between local ities in Sarawak and Sabah.

Nanga

Tekalit Pesu Segaham Danum

Marak ‘.

Parak Mendolong Purulon

Labang 180 35 77 565

485 295 340

Nanga Tekalit 166 125 640 615 425

475

Pew 56 540

475 285 330

Segaham 555 500 305

350

Danum 210 275

250

Marak Parak

185 145

Mendolong

45

relative to the stations. We recorded or captured every frog seen as we waded

upstream (see Appendix B). The Sungai Seran at Labang (see Appendix A)

was too silty for wading and was searched from boats.

At Nanga Tekalit in 1962/63 we marked, released, and recaptured frogs on

three streams - Ensurai, Sekentut, and Serbong. To avoid the bias of counting

the same frog many times, we used the number of individuals seen (either in a

quarter or during the entire year) rather than number of observations of those

species marked and released.

Table 1 gives the number of transects and number of individuals per stream

per year. Intervals between transects for Nanga Tekalit in 1962/63 are given

elsewhere (Inger & Greenberg 1966). Intervals in other years and at other

places varied according to the lengths of the sampling periods (see Appendix

A).

Statistical analysis

We relied on two measures of overlap to assess the similarity between

samples. The first of these, overlap of abundance arrays, uses Morisita’s index

as modified by Horn (1966)

C = 2CnunJ(h, + h,)N,Nz

where nji = number of individuals of species i in sample j and

hj = cnj,‘/Nj2

Wolda (1981) found this index to be relatively independent of sample size and

diversity.

The second measure of overlap, of species present in two samples, uses the

Czekanowski coefficient (Wolda 198 1) :

overlap (or similarity) = 2c/(S + L)


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414


where c = number of species common to the two samples

S = number of species in smaller sample

L = number of species in larger sample

As Wolda pointed out, most of the binary similarity coefficients have some

weaknesses, but the Czekanowski increases linearly from zero to 1.0 as c

increases, and is simple to calculate.

We have the impression that our estimate of the abundance array of the

community on a stream approaches the ‘true value’ after about five transects.

We have tested this assumption in the following way. We calculated the overlap

between two of the most heavily sampled streams at Nanga Tekalit (site 1,

Figure I), Serbong, and Ensurai, using one transect drawn at random from the

36 on each stream in 1962/63. We then recalculated the overlap after adding a

second transect drawn at random, repeating the process until we had overlaps

based on five randomly drawn transects. We followed this procedure twice.

Overlaps based on a single transect from each stream were 0.555 and 0.549 in

the two sets, increasing to 0.774 and 0.842, respectively, when two transects

were drawn from each stream, and reaching 0.812 and 0.839 after five transects.

As the last values are 95-98 of the value (0.85) obtained from the full data

set from each stream, we believe that our samples from every stream (see Table

1) in the study were adequate for our purposes.

For inter-locality measures of overlap, we summed data for a stream across all

years of sampling before calculating overlaps of abundance arrays with another

stream. We assessed the effect of this procedure on the overlaps between the

Palum Tambun at Danum, Sabah (site 8, Figure l), and each of the three

streams at Nanga Tekalit, Sarawak, sampled during three years. Consequently,

for the overlap of Palum Tambun (sampled 1986, 1989, 1990) with Sekentut

(sampled 1962, 1970, 1984) we had nine new overlap values, and nine between

Palum Tambun and Ensurai and between Palum Tambun and Serbong. For

the Palum Tambun/Sekentut pair, the mean of the nine overlaps was 0.61

(SD = 0.11) compared with 0.65 when all years for a stream were combined.

For Palum Tambun/Serbong the mean of nine was 0.5 1 (SD = 0.14) compared

to 0.51 for years combined. The mean of nine for Palum Tambun/Ensurai, 0.44

(SD = 0.1 l), diverged further from the value for years combined, 0.54, but still

close enough to justify combining years.

RESULTS AND DISCUSSION

Over short (within locality) or long distances (between localities), variation

among these riparian frog communities might appear because of differences in

general topography or vegetation, rainfall regimes (between localities), or phys-

ical characteristics of streams (gradient, width, bottom characteristics, etc.).

However, before accepting any observed differences between a pair of commu-

nities as reflecting inter-community variation, it is necessary to consider that a


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415

single community might vary over time. If the variation between two communit-

ies is no greater than the variation over time within one of them, then the

observed difference between the two communities may have only transient bio-

logical significance. We therefore begin our analysis with an examination of

variation within communities.

Our analysis has the following organization: (i) Variation over time within

a stream, thus holding stream characteristics (width, gradient, etc.) and general

environment constant, but allowing for the effects of temporal variation in rain-

fall and species’ behaviour over shorter (year) periods.

(ii) Variation between streams at a locality, thus holding general environment

(topography and vegetation) relatively constant but allowing for effects of differ-

ences in stream characteristics. (iii) Comparison of the effects of time and dis-

tance within a locality. This comparison is restricted to four streams at Nanga

Tekalit that are similar in gradient, width, and bottom types, thus minimizing

the effects of stream characteristics. (iv) Variation between communities over

greater distances (i.e. at different localities), thus allowing for effects of differ-

ences in general environment (topography and vegetation, rainfall) and in

stream characteristics (width, gradient, etc.).

Variation within localities

Nanga Tekalit (site 1, Figure 1). This is our largest data set in terms of numbers

of individuals, numbers of streams, numbers of transects, and length of observa-

tion time (Table 1). We use variation in it, among other things, as a standard

against which to evaluate variation at other localities and overlaps between

localities.

(i) Variation over time. If the assemblage of species and individuals on a

stream varies over time, there should be gradual, if not continuous, divergence

from an initial observed state. Under this hypothesis, within-stream overlaps

of abundance arrays and species occurrences between adjacent quarters of a

year should be larger than overlaps between non-adjacent quarters. We test

this prediction with the data from 1962/63 on the four larger streams at Nanga

Tekalit (Table 3), the streams for which we have most data during that year.

Table 3. O verlap of abundance arrays and of spe cies occurrences between quarters within streams at Nanga

Tekalit, Sarawak, in 1962 and 1963.

Overlap of Abundan ce Arrays Overlap of Spe cies Occurrences

Quarters

Ensurai

Sekentut Serbong Selubok Ensurai Sekentut Serbong Selubok

1x2 0.92 0.93 0.98 0.84 0.81 0.73 0.83 0.76

2X3 0.98 0.93 0.82 0.84 0.80 0.86 0.92 0.84

3x4 0.96 0.96 0.91 0.93 0.87 0.96

1X3 0.91 0.94 0.86 0.90 0.73 0.74 0.81 0.85

2X4 0.94 0.91 0.81 0.73 0.79 0.88

1x4 0.90 0.89 0.86 0.73 0.80

0.79


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416


These are also the streams most similar in width, bottom types, and gradient.

Overlaps of abundance arrays between adjacent quarters were slightly greater

than between non-adjacent quarters,

but the difference is not significant

(Mann-Whitney test, single-tailed, P = 0.09). However, overlaps of species

occurrences between adjacent quarters are significantly larger than those

between non-adjacent quarters (Mann-Whitney test, single-tailed, P = 0.025).

Of the 16 species absent from these streams in one or several quarters (i.e.

those that depressed between-quarter overlaps of species occurrences), nine

were represented by


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Variation among frog communities 417

Tab le 5. Overlap of abundan ce arrays and of spe cies occurrence s between streams at Nanga T ekalit, Sara-

wak. The rows for Selubok and Lawan are omitted due to empty cel ls in 1970 and 198 4.

Overlap of Abund ance Arrays Overlap of Spe cies Occurrences

1962 Sekentut Serbong Selubok Lawan Wong Sekentut Serbong Selubok Lawan Wong

Ensurai

0.96 0.85 0.92 0.52 0.38

0.76

0.78 0.76 0.74

0.89

Sekentut 0.87

0.88 0.53 0.29 0.78 0.80 0.64 0.70

Serbong

0.85 0.69 0.29

0.80 0.62 0.73

Selubok

0.45 0.28

0.71 0.76

Lawan

0.42

0.82

Overlap of Abund ance Arrays

Overlap of Spe cies Occurrences

1970 Sekentut Serbong Selubok Lawan Wong Sekentut Serbong Selubok Lawan Wong

Ensurai 0.71 0.71 0.77 0.73 0.89 0.67

Sekentut 0.68

0.84

0.80 0.79

Serbong 0.77

0.79



1984 Sekentut Serbong Selubok Lawan Wong

Sekentut Serbong Selubok Lawan Wong

Ensura i 0.82 0.79

0.55 0.81

0.87 0.59

Sekentut 0.95

0.41

0.76

0.69

Serbong 0.42

0.58

Tab le 6. Overlap of abunda nce arrays and of spe cies occurrence s between streams at Nanga Tekalit, Sara-

wak. Observations for each stream are summ ed over all years.





Ensura i 0.92 0.83

0.95 0.43 0.44 0.83 0.88

0.79 0.85 0.94

Sekentut 0.88 0.90 0.42 0.35 0.91 0.86 0.73 0.85

Serbong

0.87 0.38 0.33

0.86 0.84 0.90

Selubok

0.45 0.37 0.73 0.81

Lawan

0.45 0.83

Serbong (Tables 5 and 6), despite the fact that Selubok and Sekentut were

much closer to Wong (see Appendix A).

Wong and Lawan were only half the widths of the other four streams and

had much lower overlaps of abundance arrays with the four larger ones than

the last had with each other (Table 6). Except for width, Lawan was very

similar to Selubok and Sekentut, having a bottom mainly of sand and gravel,


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418


with open pools, rifIles, and side pools. In terms of microhabitats known to be

used by five dominant species (Inger 1969), Rana blythi, R. ibanorum, R. chalconota,

R. signata,

and

Pedostibes hosei,

for larval development (Inger

et al.

1986) and for

adult perch sites (Inger 1969), Lawan should have had very high overlap of

abundance arrays with Sekentut and Selubok. Its low overlap of abundance

arrays with those streams suggests that it provided a significantly different

environment, particularly for the larger species, such as R. b&hi and R. ibanorum.

These two species constituted 6 and 5 , respectively, of the Lawan sample

but 23-25 and 12-22 of the samples from Sekentut and Selubok (see

Appendix B; authorization for species’ names is also given here). These large

species also had low abundances (3 and 7 ) respectively) on Wong.

However, more than stream size was involved, for the two small streams,

approximately the same size, had a low overlap of abundance arrays with each

other. Wong had the steepest gradient of all the streams at Nanga Tekalit,

which may explain why

Lefitobrachella mjobergi,

a riflle breeding species (Inger

1985), was one of the more abundant species on Wong but was seen only once

on three of the larger streams and not on the others. Staurois natator, a frog that

in our experience perches on rocks or leaves overhanging streams, constituted

25 of the sample from Wong, but less than 1 of the other five samples.

Overlaps of species occurrences did not show a dichotomy between the small

and large streams. Although there was not complete correspondence between

the species seen on the small streams with those on the large ones, the streams

were close enough for any species in the area to reach them. Species that did

not or could not maintain sizeable populations on the small streams, i.e. those

that depressed overlap of abundance arrays, none the less contributed to overlap

of species occurrences.

(iii) Comparison of the effects of time and the unique qualities of each stream.

The Nanga Tekalit data set allows comparison of small-scale time and distance

(as represented by the distinct assemblage on each stream) effects. For this

purpose we use data only from the four larger streams to increase the time

range (Table 1) and to avoid the complicating effects of differences in stream

size. Overlaps of abundance arrays between streams within quarters (range

0.69-0.91, median = 0.84) were smaller than overlaps between quarters within

streams (median = 0.91, Table 3) (Mann-Whitney test, two-tailed, P C 0.01).

At these scales, between-stream effects contributed more to variation than time.

Expanding the time scale changed the results. The overlaps between years

within streams (Table 4) did not differ from overlaps between streams within

years (Table 5) (M ann-Whitney test, two-tailed, P > 0.10). Overlaps of species

occurrences between streams within time intervals (quarters or years) did not

differ from overlaps between time intervals within streams (Mann-Whitney

tests, P > 0.10).

Other multi-year and multi-stream samples.

Within-stream overlaps of abundances

at l-4 y at Danum (site 8) (Table 7), Purulon (site 6; 0.87, 0.93), and Men-


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419

Table 7. Overlap of abundance arrays and of spec ies occurrences between years within

streams at Danum, Sarah.

Years


Palum Sapat

Cabin Tambun Kalison W6S5

Overlap of Spec ies Occurrences

Palum Sapat

Cabin Tambun Kalison W6S5

1986x 1989 0.85 0.68 0.77 0.72

1986x 1990 0.96 0.72 0.83 0.76

1969x 1990 0.90 0.80 0.74 0.64 0.83 0.76 0.86 0.83

dolong (site 5; 0.84, 0.93, 0.94) ranged from 0.64 to 0.96 (median = 0.85). As

a set, they are smaller than the overlaps between quarters at Nanga Tekalit

(Mann-Whitney test, single-tailed, P = 0.03), but did not differ from those

between longer intervals at Nanga Tekalit (Mann-Whitney test, P > 0.20).

Within-stream overlaps of species occurrences between years at Danum, Puru-

lon (0.74, 0.84), and Mendolong (0.65-0.86) did not differ significantly from

those at Nanga Tekalit (Mann-Whitney tests, P > 0.10).

Between-stream overlaps of abundances and of species occurrences at Puru-

lon (0.97 and 0.89, respectively) were much higher than between streams at

Danum (Table 8). The two streams at Purulon joined near the origins of the

surveyed sections and were very smiliar in size, gradient, bottom substrate, and

frequency of microhabitat types.

At Danum between-stream overlaps of both abundance arrays and species

occurrences (Table 8) fell within the range of those among streams at Nanga

Tekalit. As at Nanga Tekalit, distance between streams at Danum, varying

between 1 and 12 km, did not account for differences in overlaps of abundances

between streams. The Palum Tambun was much farther from the Cabin stream

and Sepat Kalisan than from the stream at W6S5, yet had higher overlaps with

the first two. Physical differences between these streams are not clearly related

to their overlaps. All streams had mixtures of pools, riffles, and torrents, though

W6S5 had a steeper gradient. Danum was the only site besides Nanga Tekalit

where the data permitted a comparison of time and distance effects. Between-

Table 8. Overlap of abundance arrays and of spec ies occurrences between streams at

Danum, Sabah.


Palum Sapat

Tambum Kalison W6S5

Overlap of Spec ies Occurrences

Palum Sapat

Tambun Kalison

W6S5

Cabin 0.73 0.65 0.84 0.76 0.83 0.74

Palum Tambur 0.83 0.65 0.83 0.90

Sapat Kaliso n 0.57 0.82


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420


year, within-stream overlaps both of abundance arrays and species occurrences

(Table 7) were significantly higher than between-stream, within-year overlaps

(Mann-Whitney tests, two-tailed, P < 0.05).

Summa? of in&a-locality variation

(1) Within-stream overlaps (abundance arrays and species’ occurrences)

between short intervals (3 months) were very high (tested at Nanga Tekalit

only).

(2) Within-stream overlaps between years were also high (four localities), but

at Nanga Tekalit were not as high as overlaps between 3-month intervals.

(3) Between-stream overlaps (abundance arrays and species’ occurrences) were

strongly affected by stream width and gradient.

(4) If stream characteristics did not vary, overlaps (abundance arrays and

species’ occurrences) between streams within years did not differ from over-

laps between years within streams. This comparison was possible only at

Nanga Tekalit.

Variation between localities

Values of inter-locality, between-stream overlaps of abundance arrays had a

very broad range, 0.01-0.83 (Tables 9, 10, ll), and represent a significant

shift downward from intra-locality overlaps. Inter-locality overlaps of species

occurrences followed the same pattern; the range was broad and 81 of the

values fell below the range of intra-locality overlaps.

Effects of stream character.

Between-stream overlaps of abundance arrays at

Nanga Tekalit were affected by stream width. Stream width appears to have

been an important factor in inter-locality overlaps as well. We have grouped

streams (Table 1) into four size categories (map numbers in parentheses): width

3-6 m: Marok (2), Wong (l), Lawan (1); width 7-9 m: Purulon (6), Kilampon

Table 9. Overlap of abundance arrays and of spec ies occurrences between streams between loca lities in

Sarawak. Stream data were sum med over all years.

Overlap of Abundance Arrays Overlap of Spec ies Occurrences

Segaham Pesu Labang Segaham Pesu Labang

Locality Stream Segaham Marok

Pesu Seran

Segaham Marok Pesu Seran

Nanga Ensurai 0.37 0.10 0.54 0.28 0.72 0.60 0.60 0.47

Tekalit Sekentut 0.29 0.12 0.70 0.36 0.78 0.64 0.63 0.49

Selubok 0.29 0.12 0.44 0.30 0.68 0.59 0.59 0.43

Serbong 0.24 0.09 0.59 0.26 0.70 0.57 0.60 0.46

Lawan 0.45 0.22 0.25 0.26 0.60 0.42 0.55 0.39

Wong 0.22 0.27 0.22

0.16 0.71 0.66 0.62 0.38

Segaham Segaham 0.26 0.12 0.60 0.44

Marok 0.07

0.04 0.56 0.41

Pesu Pesu

0.67 0.61

.


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Table 10. Overlap of abundance arrays and of species occurrences between streams between localities in Sabah. Stream data were summed over all years.

s

2.

OVERLAP OF ABUNDANCE ARRAYS OVERLAP OF SPECIES OCCURRENCES

z?.

s

Mmak Mendolong Purulon Ma&& Mendolong

Purulon s

Locality Stream Surinsin Mendolong Purulon Kilampon surinsin

Mendolong Pundon Kilampon

s

T

Danum Cabin 0.21 0.65

0.83 0.83 0.45 0.67 0.59 0.61 2

P. Tambun 0.19

0.39 0.57 0.55 0.54 0.63 0.67 0.63

S. Ka.lison 0.09 0.37 0.56 0.54

0.40

6

0.65 0.58

w6S5 0.18

0.60

0.49

0.80 0.78 0.48 0.72 0.65

g

Marak Parak

0.67

0.15 0.29 0.24

0.67 0.71 s

Mendolong

0.60

0.68 0.63 0.84

N.

0.80 -g.


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Table 11. Overlap of abundance arrays and of species occurrences between streams between localities in Sabah and Sarawak. Stream data were summed over all

years.

OVERLAP OF ABUNDANCE ARRAYS

SABAH LOCALITIES

Danum

Mamk Mendolong Purulon

Sarawak

Localities Stream Cabin P. Tambun

S. Kaiison W6S5 Surinson Mendolong Purulon Kilampon

Labang Seran 0.19 0.21 0.20 0.08 0.01

Nanga

0.07 0.02

Ensurai 0.30 0.54

0.01

0.48 0.15 0.02 0.09

Tekalit

0.03

Sekentut 0.34

0.02

0.65 0.63 0.18 0.03 0.09

Selubok

0.04

0.30 0.54

0.04

0.45 0.16 0.02 0.09

Serbong 0.30

0.03 0.02

0.51 0.57 0.16 0.02 0.09

Lawan

0.04

0.38 0.29

0.04

0.30 0.33 0.02 0.15

Wong

0.10

0.27

0.07

0.27 0.52 0.30

Pesu

0.04

Pesu

0.28

0.24

0.25

0.42

0.18

0.54 0.14 0.03 0.06 0.04

0.06

Segaham Segaham 0.16 0.14 0.17 0.11 0.09 0.07

Marok 0.20

0.10

0.27

0.08

0.16 0.44 0.03 0.09 0.17

0.14

OVERLAP OF SPECIE S OCCURRENCES

SABAH LOCALITIES

Danum

Mart& Mendolong Purulon

Sarawak

Localities Stream Cabin P. Tambun S. Kalison

W6S5 Surinson Mendolong Purulon Kilampon

Labang Seran

0.38 0.43 0.44 0.40

Nanga

0.15

Ensurai

0.65

0.28

0.67

0.24

0.68

0.28

0.70 0.43

Tekalit

0.60

Sekentut

0.65

0.53

0.67 0.63

0.60

0.60 0.52 0.54

Selubok

0.49 0.62

0.56 0.54

0.59 0.55 0.39 0.49

Serbong

0.62

0.46

0.59

0.65

0.49

0.57 0.42 0.56

Lawan

0.61

0.49

0.59

0.51

0.65 0.56 0.40

Wong

0.68

0.50

0.65

0.42

0.71

0.50

Pew

0.64

Pesu

0.46 0.62

0.56

0.60

0.49

0.66

0.60 0.51 0.33

Segaham

0.45

Segaham 0.61

0.42

0.59

0.55

0.40

0.51 0.40

Marok

0.50

0.41

0.53

0.50

0.45

0.51 0.52 0.36 0.51 0.54

0.47

I

rlrt

~.


15/25


423

(6), Cabin (8), W6S5 (8), Sepat Kalisan (8); width 10-14 m: Pesu (3), Seran

(4), Mendolong (5)) P

a urn Tambun (8), and the four larger streams at Nanga

Tekalit (1); width 25 m: Segaham (2). If stream width accounts for a significant

part of the inter-locality variation, overlaps between streams within size categor-

ies should be greater than overlaps between streams across size categories.

Overlaps (grouped into four classes:

cO.21, 0.21-0.40, 0.41-0.60, BO.60)

within-stie categories were significantly greater than those across size categories

(chi-square = 19.4, df = 3, P < 0.01); 57 of the within-size category overlaps

(n = 30) exceeded 0.40 compared to 17 of the between-size overlaps (n =

82).

Between-stream overlaps at Nanga Tekalit showed some effect of differences

in stream gradients. If differences in gradients affect inter-locality overlaps,

overlaps between streams of similar gradients should exceed those between

streams of differing gradients. We grouped streams into the following gradient

classes from steepest (A) to flat (E); A: M arok, Purulon, Kilampon, Mendolong;

B: Surinsin, Segaham; C: W6S5, Wong; D: Pesu, Lawan, Ensurai, Sekentut,

Selubok, Serbong, Cabin, Palum Tambun, Sepat Kalisan; E: Seran. Overlaps

were grouped as in the preceding paragraph. Overlaps within gradient classes

were significantly larger than those across classes (chi-square = 26.31, P <

0.01); 53 of the within-class overlaps (n = 30) exceeded 0.40, in contrast to

14 (n = 99) of the between-class overlaps.

Inter-locality overlaps of species occurrences gave slightly different results.

Overlaps within-and between-width classes did not differ (chi-square = 4.94,

P = 0.30). However, overlaps within gradient classes were significantly greater

than overlaps between those classes (chi-square = 12.44, P < 0.02). We inter-

pret these results as indicating that stream gradient had a greater effect than

stream width on the occurrences of species.

The effect of stream gradient is best seen on the Seran, the only stream

flowing through flat forest and the only one with turbid water and a silt bottom.

These circumstances almost certainly account for the absence of any of the 15

species (27 of 55) in our data set that breed at riffles and torrents and have

larvae that either attach to rocks or wriggle into interstices between rocks and

gravel on stream bottoms. These 15 include all five species of

Amolops

(Inger

1966), three species of Ansonia (Inger 1992) four species of Leptobrachella, and

three species scattered through other genera (Inger 1985, and unpublished

data). An additional five species absent along the Seran have been observed

elsewhere only at turbulent, rocky areas of other streams: Micrixalus baluensis,

Philautus hosei, Rana hosei, Staurois latopalmatus, S. tuberilinguis (unpublished data).

The two streams at Segaham (Figure 1, locality 2) show interaction of stream

width and gradient on overlap. Although the two streams, Marok (3 m) and

Segaham (25 m), joined where they were sampled, their overlap of abundance

arrays was only 0.07 and, though their overlap of species occurrences was higher

(0.65) it was still lower than the overlaps at Nanga Tekalit. The five largest

species at that locality were much more abundant on the Segaham (41 of the


16/25

424


sample) than on the Marok (8 ). Both are high gradient streams. However,

the Marok consists of a series of small waterfalls separated by short pools over

gravel and rock, whereas the Segaham has long stretches of foaming rapids over

large boulders, the kind of habitat that supports populations of adult Rana hosei

and Amolops cavitym~anum and is used by tadpoles of A. cavi~mpanum and Bufo

juxtasper. The last two species were five times more abundant and Rana hosei 20

times more abundant on the Segaham than on the Marok (Appendix B).

Effects of rainfall patterns. Another environmental factor that may have played

a role is the pattern of local rainfall. Variation in rainfall locally may have

affected overlaps over time within streams, and systematic differences between

localities in amount and seasonal distribution of rainfall may have affected

inter-locality overlaps. Several features of the climate of Borneo are important

here: (1) At any given site, in the great majority of years there are no months

totally lacking rain. For example, over a 30-year period at Melalap Estate, a

recording station 10 km from Purulon (site 6), no month lacked rain and only

two had 25 mm, which was enough

to cause spates on the observation streams, were distributed at random through

the year (Lloyd et al. 1968). Rainfall was moderately heavy during the other

sampling periods at Nanga Tekalit and overlaps of abundance arrays between

years remained high (Table 4). The fact that sampling periods at Nanga Tekalit

over the years did not occur during the same calendar intervals appears to have

had little effect. Within-stream, between-year overlaps using data from the

entire year 1962/63 did not differ from overlaps using data only from those


17/25


RAIN IN

mm (1887)

500

w MELALA P u MENDOLONG w DANUM

J F MAMJJASOND

MONTH

RAIN IN mm

(1908)

1000

+ Nanga T ekallt 1963 q MELALAP

JFMAMJJASOND

MONTH

RAIN IN m m (WSO)

700

td MELALA P i-i MENDOLONG

n

DANUM

J F M A M J JASOND

MONTH

4 5

Figure 2. Monthly rainfall data for three years at three localiti es in Sabah. Melalap is 8 km from our

sampled locality Purulon. The middle graph gives the monthly rainfall for Nanga Tekalit (Sarawak) in

1962163.


18/25

426


parts of 1962/63 matching the periods of work in 1970 and 1984 (Wilcoxon

matched-pairs signed-ranks test, P > 0.05).

Although rainfall varied appreciably from year to year at Danum (Figure 2)

and during sampling periods, there was no association between rainfall and

amount of overlap within streams (Table 7). At Purulon rainfall during the

second sampling period was less than 30 that in the first period (see above),

yet overlaps between years were very high (0.87, 0.92). Similarly, at Mendolong

between-year overlaps were high (0.84-0.94) despite variation in rainfall.

If differing amounts of rainfall (either at the time of sampling or annually)

affect inter-locality overlaps significantly, overlaps between localities having

similar rainfall should be larger than those between localities differing in

amounts of rain. To test this hypothesis, holding stream gradient and width

constant, we compare overlaps of abundance arrays between the four larger

streams at Nanga Tekalit and Pesu (site 3), both areas with high rainfall, with

overlaps between those streams and Palum Tambun at Danum (about half as

much rain). Differences between the two sets of overlaps (see Tables 9 and 11)

do not differ significantly (Mann-Whitney test, P > 0.20). All other inter-

locality tests of rainfall effects are confounded by differences in gradient or

stream width. However, overlaps of abundance arrays between Purulon and

Mendolong (twice as much rain) were high (BO.60) despite differences in

stream width. Also overlaps between Purulon streams and those at Danum

(twice as much rain) were also high (0.54-0.83, Table 10) despite differences

in gradient.

Restricted geographic distributions.

In all the preceding analyses, a tacit assump-

tion is that all species are available at all localities. There is evidence, on the

contrary, that some species have limited geographic distributions within

Borneo. For this part of the analysis, we use all frogs observed at a locality,

whether on a surveyed stream or not, to establish presence in an area. General

distribution is based on Inger ( 1966), Inger & Dring ( 1988), Inger & Stuebing

(1992) and Matsui (1986). Ab un d antes and distributions of species mentioned

below are given in Appendix B.

One of the dominant species along streams in hilly areas of Sarawak,

Rana

ibanorum,

is currently known only from Sarawak. Intensive, repeated search at

Danum (site 8) in streams that provide appropriate habitats (clear streams

having beds of sand, gravel, and rock) and at other similar streams 100 km

south and 175 km west of Danum (field work by Inger) have failed to uncover

this species in eastern Sabah.

Bufo asper,

abundant on streams at all four localit-

ies in Sarawak, was also absent at Danum and the eastern Sabah localities

referred to above, again, despite the presence of appropriate habitats. Other

abundant stream-side species that appear to have geographically restricted dis-

tributions, despite wider availability of suitable habitat, include Amolops phaeom-

eluS (found in central Sarawak) and

A. whiteheadi

(western Sabah). Altogether,

11 species (20 )

in our data set depress inter-locality overlaps because of

geographically, as distinguished from ecologically, restricted distributions.


19/25


427

Do these restricted ranges reflect historical processes or competitive interac-

tions with ecologically similar species? We look for evidence of biotic interac-

tions within groups of closely related species, which, as they are usually ecolo-

gically homogeneous, are most likely to show competition. There were eight

such groups in our sample, four of which were present in sufficient numbers

for statistical analysis.

1. Rana ibanorum co-occurred with two related large species along streams at

Nanga Tekalit (site 1) (Inger & Greenberg 1966). All three were absent from

four streams in western Sabah that lacked suitable microhabitat. Correlations

of relative abundances of these species in the 14 streams where at least one

was present were positive. This suggests that the absence of

R. ibanorum

from

appropriate habitat in eastern Sabah is independent of the distribution of the

other two species.

2. The two large species of

Bufo,

usper and

juxtasper,

which form a distinct

species group (Inger 1972), co-occurred on seven streams. As their abundances

were negatively correlated (Spearman r, = -0.57, P < O.Ol), the absence of B.

asper from its usual habitat in eastern Sabah could be the result of competition.

3.. The two species of Amolops having geographically restricted distributions

(see above),.each co-occurred with an abundant congener, poecilus in the case of

phaeomeru&nd orphnocnemis in the case of whiteheadi. Larvae of phaeomerus and

poecilus

have been collected together in tadpole stations (Inger 1985) as have

tadpoles of the other two (unpublished data). Relative abundances of

whiteheadi

and

orphnocnemis

were positively correlated, whereas abundances of

phaeomerus

and

poecilus

were negatively correlated though not at a significant level (P >

0.05). The distributions of

whiteheadi

and

phaeomerus

were not completely comple-

mentary as neither occurred in eastern Sabah.

4. The three species of Staurois (Appendix B) co-occurred in four streams and

in pairs or singly in the remaining 14 streams. Their relative abundances were

positively correlated, which makes competition an unlikely explanation of the

absence of S. tuberilinguis from streams at Danum and other streams in eastern

Sabah that lie outside our study area.

The other groups having one or more species with geographically restricted

ranges had small sample sizes (Appendix B). They include: three species of

slender toads,

Ansonia,

one widely distributed and two absent from eastern

Sabah though sympatric at two localities in Sarawak; two species of horned

frogs,

Megophy,

one apparently restricted to central Sarawak and sympatric

with the second which was observed across the study area; and three species

of small pelobatid toads, Leptobrachella, with one restricted to Sabah and two

to Sarawak. As a genus, Leptobrachella exhibits strong altitudinal stratification

(Inger & Stuebing 1992), suggesting that in this group competition may be

important, if not universal. The other two groups show no evidence that biotic

interactions play a role in their geographic restrictions.

According to Hanski (1982)) for many organisms there is a positive correla-

tion between local abundance and regional distribution; i.e. species tend to be

either locally abundant and widespread (‘core species’) or locally rare and


20/25

428


regionally scarce (‘satellite species’). An earlier paper (Inger 1969) on the frogs

of the streams at Nanga Tekalit noted that nine species accounted for >85

of observations and each contributed >3.5 of the sample. Hanski’s model

predicts that these nine species should have been equally abundant at Danum,

where streams were very similar to those at Nanga Tekalit in width, gradient,

and array of microhabitats. Yet at Danum these nine species constituted


21/25

Variation among frog communities 429

breed in clear, turbulent water, i.e. roughly a quarter of the species in our

study.

There were significant differences within and between localities in rainfall,

both on an annual basis and at the times of sampling. Yet this variation did

not account for differences in overlaps among communities.

Although environmental factors had strong effects on inter-locality overlaps,

they do not account for all of the variation. At least 11 species have geographic-

ally restricted ranges that cannot be explained on the basis of distribution of

suitable microhabitats. Nine of these co-occur with at least one similar congener

at one or more localities. Regional processes (sensu Ricklefs 1987), perhaps the

existence or timing of barriers to dispersal or the timing of speciation events,

appear to be responsible for their geographic restrictions rather than biotic

interactions.

ACKNOWLEDGEMENTS

We wish to express our thanks to men of the Iban longhouse, Rumah Jimbong.

Without their able assistance, none of the work at Nanga Tekalit would have

taken place. We also wish to acknowledge Lucas Chin, Director, and Charles

Leh, Zoologist, both of the Sarawak Museum, who arranged for government

permits and eased many logistical problems. We are grateful to the authorities

of Sabah Parks, Sabah Forest Industries, and Yayasan Sabah for permission to

work in areas under their respective jurisdictions and for living accommoda-

tions. We are also grateful to Sabah Parks and Universiti Kebangsaan Malaysia

(Kampus Sabah) for provision of camping equipment, transportation, and

logistical assistance. We thank R. B. Stuebing, F. L. Tan, and P. Yambun for

assistance in the field and for many kindnesses. Professional colleagues, J. P.

Bacon, S. Emerson, K. J. Frogner, W. Hosmer, D. Karns, F. W. King, J. C.

Murphy, and P. Walker, helped us collect at various times. We are grateful to

M. Lloyd and B. Zimmerman for helpful comments on the manuscript. We

received valued technical assistance from A. Resetar. Field and laboratory work

were partially supported by grants from the National Science Foundation, the

Allen-Heath Memorial Foundation, and the National Geographic Society.

LITERATURE CITED

CRUMP, M. L. 1971. Quantitative analysis of the eco logica l distribution of a tropical herpetofauna. Occa sional

Papers, Mwum

qf

Natur Histoy, University of Kan sas 3~1-62.

DUELLMAN, W. E. & LYNCH, J. D. 1969. Description s

ofhlopus

tadpoles and their relevance to atelopo-

did class ificatio n. Herpetologica 25~231-240.

GASCON, C. 1991. Popu lations and community-level analyses of spe cies occurrences of Central Amazonian

rainforest tadpoles. Ecology 72: 1731-l 746.

HANSK I, I. 1982. Dynamics of regional distribution: the core and satellite spec ies hypothesis. Oikos 38:210-

221.

HEYER , W. R. 1973. Eco logica l interactions of frog larvae at a seaso nal tropical location in Thailand.Jo anzal

of HerpGtologr 7~337-3 61.


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430


HORN, H. 1966. The measurement of ‘overlap’ in comparative ecolo gical studies . American Naturalist 100:419-

424.

INGER, R. F. 1966. The systema tics and zoogeography of the Amp hibia of Borneo. Ficldiuna : Zoology 52:1-

4Q2.

INGER, R. F. 1969. Organization of comm unities of frogs along sma ll rain forest streams in Sarawak. Journal

of Anim al Ecology 38123-148.

INGER, R. F. 1972. Bufo of Eurasia. Pp. 108-l 18, 357-360 in Blair, F. W. (ed.). Evolution in the genus Bufo.

s.

University of Texas Press, Austin.

INGER, R. F. 1985. Tadp oles of the forested regions of Borneo. Fieldiana: Zoology (n.s.) 26:1-89.

INGER, R. F. 1992. Variation of apomorph ic characters in stream-dwelling tadpoles of the bufonid genus

Anso nia (Amphibia: Anura). Zoolog ical Journal of the Linncan Society 105:225-237.

INGER, R. F. & COLWELL, R. K. 1977. Organization of contiguo us comm unities of amp hibians and

reptiles in Thailan d. Eco logic al Morwgraphr 47~229-253.

INGER, R. F. & DRING, J. 1988. Taxonom ic and ecolo gical relations of Bornean stream toads allied to

Anso nia leptopus (Guenther) (Anura: Bufonidae). Malayan Nature Journal 419:461-471.

INGER, R. F. & GREENBERG, B. 1966. Eco logic al and competitive relations among three spec ies of frog

(genus Rana). E cology 47~746-759.

INGER, R. F. & STUEBING , R. B. 1991. Frogs of Sabah. Sabah Parks Pub lication, no. 10.

INGER, R. F. & STUEBING , R. B. 1992. The montane amph ibian fauna of northwestern Borneo. Muluyun

Nature Journal 46:41-5 1.

INGER, R. F., VORIS, H. K. & FROGNER, K. J, 1986. Organization of a community of tadpoles in rain

forest streams in Borneo. Journal of Trop ical Ecolog y 2: 193-205.

LLOYD, M., INGER, R. F. & KING, F. W. 1968. On the diversity of reptile and amph ibian spe cies in a

Bornean rain forest. American Naturalist 102:497-515.

MATSUI, M. 1986. Three new spec ies of Amo lops from Borneo. Copeis 1986:623-630.

McDIARMID, R. W. 1978. Evolution of parental care in frogs. Pp. 127-147 in Burkhardt, G. M. & Bekoff,

M. (eds). The development of behavior: comparative and evolutionary aspec ts. STPM Press, New York.

RICKLEFS, R. E. 1987. Community diversity: relative roles of loca l and regional process es. S cienc e 235:167-

171.

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Accepted 27 April 1993

c


23/25


431

APPENDIX A. Site chara cteristics. Upper four in Sarawak, lower four in Sabah.

Site Labang Nanga Tekalit Pesu Segaham

Coordinates 3” 21’N/113” 27’E

Elevation (m) Cl00

Topography

flat

Vegetation primary forest

Streams:

number 1

widths (m) 10

gradient low

clarity turbid

bottom

mud

Dates:

first Ott 63/Feb 64 128 d

second

third

Locality 4

(Figure 1)

1” 37’N/113” 35’E

loo-230

hilly

primary forest

3“ 7’/113” 48’E


24/25

432


APPENDIX B. List of spec ies and specim ens. Authorities for spec ies names given in Inger (1966, 1985) and

Inger & Stuebing (1991).

ANURAN SPECIES

Nanga

Tekalit Segaham

Ensurai Sekentut Sex-bong Selubok Wong Lawan Segaham Marok

Amolops cavitympanum

Amolops orphnocnemis

Amolops phaeomerus

Amolops poecilus

Amolops whiteheadi

Ansonia albomaculata

Anronia leptopus

Ansonia longidigita

Ansonia spinulafer .

Bufo asper

Bufo divergens

Bufo juxtasper

Chaperina furca

Leptobrachella baluensis

Leptobrachella mjobergi

Leptobrachella parva

Leptobrachella serasanae

Leptobrachium hendricksoni

Leptobrachium montanum

Leptobrachium nigrops

Leptolalax gracillis

Megophrys edwardinae

Megophrys nasuta

Micrixalus baluensis

Microphyia petrigena

Occidoqga baluensis

Pedostibes hosei

Pedostibes rugosus

Philautus disgregus

Philautus hosei

Philautus tectus

Rana baramica

Rana bbthi

Rana chalconota

Rana glandulosa

Rana hosei

Rana ibanorum

Rana ingeri

Rana kuhli

Rana laticeps

Rana malesiana

Rana paramacrodon

Rana sign&a

Rhacophorus bimaculatus

Rhacophorus gauni

Rhacophorus pardalis

Staurois latopalmatus

Staurois natator

Staurois tuberlinguis

TOTALS

0

0 0 0

0

0 0 0

90 83 330 107

13 4

28 13

0 0 0 0

0

0 0 0

32 12 21 20

0

0 0 0

0 0

0 0

107

121 71

52 0

11

2 2 0

0 0 0

0 0 0

0 1 1

0 0 0

0 0 0

0

0 0

8

20

9

0 0

0

3

0

0

5

0

0

45

0

0

0

0

1

0

0

0

5

0

3

0

4

0 0

28

3

0 0 0 0

2 0 1 1

12 143 76 3

0 0 0 0

0 0 137

2

5 2 1 0

0 0 0

0

0 0 0 3

15 14 13 1

48 1 0 0

1

0 83 8

0 0 0 0

0 0 0 0

17 0 0 96

0 0 0 4

0 0 0 0

0 0 0 0

3 0 0 20

0 0 0 0

7 1

3 0

2 1 0

2

3 2 0 0

1

14

0

2

0

1

0

0

1

1

10 0 5 0 1

50

48 106

29

1

0 0 0 0 0

0 0 0 0 0

6 0 4 5 27

0 0 0

1

0

0 1

12

2 0 0

4 0 0

0 6 1

0 2 0

0 0 0

8 0 0

0 0 5

0 0 0 0 0

0

257

307

292 200 10 30

171 156

200 125

45 135

0 0 0 0 0

0

100 56 36 20 4 0

247 141 199 191 25 22

12 82 43 44 1 18

12 14 9 17 16 55

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

69 150 272 23 10 11

1

3

18

0

1

11

0

1

0

0

1

1

1

2

0

1281

0

7

2

7

3

0

1221

6

3

0

1664

0

10

4

3

0

0

870

4 2 5

80 15 2

7 0 0

349 468 605

0

18

70

0

117

26

3

0

0

0

0

2

0

0

11

0

14

5

0

2

0

0

&

78

2

0

0

1

0

0

1

0

7

21

292


25/25


Marak

Pew Labang Parak

Purulon Danum Mendolong

Pesu Seran Surinsin Purulon Kilampon Cabin P.Tambun SKalison W6S5 Mendolong

0 0

2 2

0 0 31

218

0 0 0

0

0 0 0 0

0 0 0

29

25:

0

0

5

0 0 0 0 3

96 161 66 108 216

0 0 0 0 0

0

0

0 0 0

0 0 0 0 161

0 0

0 0 0 0

1 0 0

0 0 1

0 0

0 0 0 0

0 0 0 0

0 0

217 27 0 1

2

0

2 0 0 0 0

1

6 0 13 53 60 3

0 0 0

3 3 0

0 0 0 0

0 0

0 00 0 0

0 0

0 0 0 0

12 4

0 0 0 0

0 0

1

0 0 0

0 0

0 2 0 6

5 0

0 2 0 0

0 0

0 0 3 18 34

14

0

0

0

0

0

0

0

0

0 0 0

5

0

6 0 4

0

0

0

0

0

0

0

0

0

60

0

0

0

1

1

241

118

315

187

5

181

10

0

T

0

0

379

18 0

0 0

0 0

0

0

0 0

14 0

38 0

57 1

155 0

0 14

0 0

61 0

0

5

0 0

1 0

9 0

7 0

5 2 3 3 8

0 0 0 0 0

2 0 0 0 0

0

15 42 12

1

0 0

0

0 0

0 0 1 0 4

0 0 0 5 0

0 0 0 0 0

0 0 0 0 0

0

20

235 83 10

1 50 48 37 33

0 0 0 0 0

1 0 0 0 0

0 0 0 0 0

0 6

1

1 0

48 30

91 17 113

0 0

0

0 0

0 0

0 0 0

0 0

0 0 0

24

14 56

82

21

5

0

19

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11

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1761

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411

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9

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136

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207

0

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9

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50

0

0

0

10

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20

73

15

514

6 5

63 6

11 0

549 276

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20

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0

2:

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22

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124

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Documents

A Comparison of Amphibian Communities Through Time and Place to Place